Author Report for: Nelson DCNo contact information in database for Nelson DC
Chen J, Nelson DC, Shukla D Ref: J Chem Inf Model, :, 2022 : PubMed ESTHER: Chen_2022_J.Chem.Inf.Model__ PubMedSearch: Chen 2022 J.Chem.Inf.Model PubMedID: 35192364 Abstract Parasitic weeds such as Striga have led to significant losses in agricultural productivity worldwide. These weeds use the plant hormone strigolactone as a germination stimulant. Strigolactone signaling involves substrate hydrolysis followed by a conformational change of the receptor to a "closed" or "active" state that associates with a signaling partner, MAX2/D3. Crystal structures of active and inactive AtD14 receptors have helped elucidate the structural changes involved in activation. However, the mechanism by which the receptor activates remains unknown. The ligand dependence of AtD14 activation has been disputed by mutagenesis studies showing that enzymatically inactive receptors are able to associate with MAX2 proteins. Furthermore, activation differences between strigolactone receptor in Striga, ShHTL7, and AtD14 could contribute to the high sensitivity to strigolactones exhibited by parasitic plants. Using molecular dynamics simulations, we demonstrate that both AtD14 and ShHTL7 could adopt an active conformation in the absence of ligand. However, ShHTL7 exhibits a higher population in the inactive apo state as compared to the AtD14 receptor. We demonstrate that this difference in inactive state population is caused by sequence differences between their D-loops and interactions with the catalytic histidine that prevent full binding pocket closure in ShHTL7. These results indicate that ligand hydrolysis would enhance the active state population by destabilizing the inactive state in ShHTL7 as compared to AtD14. We also show that the mechanism of activation is more concerted in AtD14 than in ShHTL7 and that the main barrier to activation in ShHTL7 is closing of the binding pocket. Title: The strigolactone receptor D14 targets SMAX1 for degradation in response to GR24 treatment and osmotic stress Li Q, Martin-Fontecha ES, Khosla A, White ARF, Chang S, Cubas P, Nelson DC Ref: Plant Commun, 3:100303, 2022 : PubMed ESTHER: Li_2022_Plant.Commun_3_100303 PubMedSearch: Li 2022 Plant.Commun 3 100303 PubMedID: 35529949 Abstract The effects of the phytohormone strigolactone (SL) and smoke-derived karrikins (KARs) on plants are generally distinct, despite the fact that they are perceived through very similar mechanisms. The homologous receptors DWARF14 (D14) and KARRIKIN-INSENSITIVE2 (KAI2), together with the F-box protein MORE AXILLARY GROWTH2 (MAX2), mediate SL and KAR responses, respectively, by targeting different SMAX1-LIKE (SMXL) family proteins for degradation. These mechanisms are putatively well-insulated, with D14-MAX2 targeting SMXL6, SMXL7, and SMXL8sand KAI2-MAX2 targeting SMAX1 and SMXL2 in Arabidopsis thaliana. Recent evidence challenges this model. We investigated whether D14 can target SMAX1 and whether this occurs naturally. Genetic analysis indicates that the SL analog GR24 promotes D14-SMAX1 crosstalk. Although D14 shows weaker interactions with SMAX1 than with SMXL2 or SMXL7, D14 mediates GR24-induced degradation of SMAX1 in plants. Osmotic stress triggers SMAX1 degradation, which is protective, through SL biosynthesis and signaling genes. Thus, D14-SMAX1 crosstalk may be beneficial and not simply a vestige of the evolution of the SL pathway. Title: A KARRIKIN INSENSITIVE2 paralog in lettuce mediates highly sensitive germination responses to karrikinolide Martinez SE, Conn CE, Guercio AM, Sepulveda C, Fiscus CJ, Koenig D, Shabek N, Nelson DC Ref: Plant Physiol, 190:1440, 2022 : PubMed ESTHER: Martinez_2022_Plant.Physiol_190_1440 PubMedSearch: Martinez 2022 Plant.Physiol 190 1440 PubMedID: 35809069 Abstract Karrikins (KARs) are chemicals in smoke that can enhance germination of many plants. Lettuce (Lactuca sativa) cv. Grand Rapids germinates in response to nanomolar karrikinolide (KAR1). Lettuce is much less responsive to KAR2 or a mixture of synthetic strigolactone analogs, rac-GR24. We investigated the molecular basis of selective and sensitive KAR1 perception in lettuce. The lettuce genome contains two copies of KARRIKIN INSENSITIVE2 (KAI2), which in Arabidopsis (Arabidopsis thaliana) encodes a receptor that is required for KAR responses. LsKAI2b is more highly expressed than LsKAI2a in dry achenes and during early stages of imbibition. Through cross-species complementation assays in Arabidopsis, we found that an LsKAI2b transgene confers robust responses to KAR1, but LsKAI2a does not. Therefore, LsKAI2b likely mediates KAR1 responses in lettuce. We compared homology models of KAI2 proteins from lettuce and a fire-follower, whispering bells (Emmenanthe penduliflora). This identified pocket residues 96, 124, 139, and 161 as candidates that influence the ligand specificity of KAI2. Further support for the importance of these residues was found through a broader comparison of pocket residues among 281 KAI2 proteins from 184 asterid species. Almost all KAI2 proteins had either Tyr or Phe identity at position 124. Genes encoding Y124-type KAI2 are more broadly distributed in asterids than in F124-type KAI2. Substitutions at residues 96, 124, 139, and 161 in Arabidopsis KAI2 produced a broad array of responses to KAR1, KAR2, and rac-GR24. This suggests that the diverse ligand preferences observed among KAI2 proteins in plants could have evolved through relatively few mutations. Title: Strigolactones are chemoattractants for host tropism in Orobanchaceae parasitic plants Ogawa S, Cui S, White ARF, Nelson DC, Yoshida S, Shirasu K Ref: Nat Commun, 13:4653, 2022 : PubMed ESTHER: Ogawa_2022_Nat.Commun_13_4653 PubMedSearch: Ogawa 2022 Nat.Commun 13 4653 PubMedID: 35970835 Abstract Parasitic plants are worldwide threats that damage major agricultural crops. To initiate infection, parasitic plants have developed the ability to locate hosts and grow towards them. This ability, called host tropism, is critical for parasite survival, but its underlying mechanism remains mostly unresolved. To characterise host tropism, we used the model facultative root parasite Phtheirospermum japonicum, a member of the Orobanchaceae. Here, we show that strigolactones (SLs) function as host-derived chemoattractants. Chemotropism to SLs is also found in Striga hermonthica, a parasitic member of the Orobanchaceae, but not in non-parasites. Intriguingly, chemotropism to SLs in P. japonicum is attenuated in ammonium ion-rich conditions, where SLs are perceived, but the resulting asymmetrical accumulation of the auxin transporter PIN2 is diminished. P. japonicum encodes putative receptors that sense exogenous SLs, whereas expression of a dominant-negative form reduces its chemotropic ability. We propose a function for SLs as navigators for parasite roots. Title: KARRIKIN UP-REGULATED F-BOX 1 (KUF1) imposes negative feedback regulation of karrikin and KAI2 ligand metabolism in Arabidopsis thaliana Sepulveda C, Guzman MA, Li Q, Villaecija-Aguilar JA, Martinez SE, Kamran M, Khosla A, Liu W, Gendron JM and Nelson DC <2 more author(s)> Sepulveda C, Guzman MA, Li Q, Villaecija-Aguilar JA, Martinez SE, Kamran M, Khosla A, Liu W, Gendron JM, Gutjahr C, Waters MT, Nelson DC (- 2) Ref: Proc Natl Acad Sci U S A, 119:e2112820119, 2022 : PubMed ESTHER: Sepulveda_2022_Proc.Natl.Acad.Sci.U.S.A_119_e2112820119 PubMedSearch: Sepulveda 2022 Proc.Natl.Acad.Sci.U.S.A 119 e2112820119 PubMedID: 35254909 Abstract Significance: Karrikins are chemicals in smoke that stimulate regrowth of many plants after fire. However, karrikin responses are not limited to species from fire-prone environments and can affect growth after germination. Putatively, this is because karrikins mimic an unknown signal in plants, KAI2 ligand (KL). Karrikins likely require modification in plants to become bioactive. We identify a gene, KUF1, that appears to negatively regulate biosynthesis of KL and metabolism of a specific karrikin. KUF1 expression increases in response to karrikin or KL signaling, thus forming a negative feedback loop that limits further activation of the signaling pathway. This discovery will advance understanding of how karrikins are perceived and how smoke-activated germination evolved. It will also aid identification of the elusive KL. Title: Karrikin perception and signalling Waters MT, Nelson DC Ref: New Phytol, :, 2022 : PubMed ESTHER: Waters_2022_New.Phytol__ PubMedSearch: Waters 2022 New.Phytol PubMedID: 36333982 Abstract Karrikins are a class of butenolide compounds found in smoke that were first identified as seed germination stimulants for fire-following species. Early studies of karrikins classified the germination and post-germination responses of many plant species, and investigated crosstalk with plant hormones that regulate germination. The discovery that Arabidopsis thaliana responds to karrikins laid the foundation for identifying mutants with altered karrikin responses. Genetic analysis of karrikin signalling revealed an unexpected link to strigolactones, a class of carotenoid-derived plant hormones. Substantial progress has since been made toward understanding how karrikins are perceived and regulate plant growth, in no small part due to advances in understanding strigolactone perception. Karrikin and strigolactone signalling systems are evolutionarily related and retain a high degree of similarity. There is strong evidence that karrikins (KARs) are natural analogues of an endogenous signal(s), KAI2 ligand (KL), which remains unknown. KAR/KL signalling regulates many developmental processes in plants including germination, seedling photomorphogenesis, and root and root hair growth. KAR/KL signalling also affects abiotic stress responses and arbuscular mycorrhizal symbiosis. Here we summarise the current knowledge of KAR/KL signalling, and discuss current controversies and unanswered questions in this field. Title: Rapid analysis of strigolactone receptor activity in a Nicotiana benthamiana dwarf14 mutant White ARF, Mendez JA, Khosla A, Nelson DC Ref: Plant Direct, 6:e389, 2022 : PubMed ESTHER: White_2022_Plant.Direct_6_e389 PubMedSearch: White 2022 Plant.Direct 6 e389 PubMedID: 35355884 Abstract DWARF14 (D14) is an /beta-hydrolase and receptor for the plant hormone strigolactone (SL) in angiosperms. Upon SL perception, D14 works with MORE AXILLARY GROWTH2 (MAX2) to trigger polyubiquitination and degradation of DWARF53(D53)-type proteins in the SUPPRESSOR OF MAX2 1-LIKE (SMXL) family. We used CRISPR-Cas9 to generate knockout alleles of the two homoeologous D14 genes in the Nicotiana benthamiana genome. The Nbd14a,b double mutant had several phenotypes that are consistent with the loss of SL perception in other plants, including increased axillary bud outgrowth, reduced height, shortened petioles, and smaller leaves. A ratiometric fluorescent reporter system was used to monitor degradation of SMXL7 from Arabidopsis thaliana (AtSMXL7) after transient expression in N. benthamiana and treatment with the strigolactone analog GR24. AtSMXL7 was degraded after treatment with GR24(5DS), which has the stereochemical configuration of natural SLs, as well as its enantiomer GR24 (ent-5DS). In Nbd14a,b leaves, AtSMXL7 abundance was unaffected by rac-GR24 or either GR24 stereoisomer. Transient coexpression of AtD14 with the AtSMXL7 reporter in Nbd14a,b restored the degradation response to rac-GR24, but required an active catalytic triad. We used this platform to evaluate the ability of several AtD14 mutants that had not been characterized in plants to target AtSMXL7 for degradation. Title: The mechanism of host-induced germination in root parasitic plants Nelson DC Ref: Plant Physiol, 185:1353, 2021 : PubMed ESTHER: Nelson_2021_Plant.Physiol_185_1353 PubMedSearch: Nelson 2021 Plant.Physiol 185 1353 PubMedID: 33793958 Abstract Chemical signals known as strigolactones (SLs) were discovered more than 50 years ago as host-derived germination stimulants of parasitic plants in the Orobanchaceae. Strigolactone-responsive germination is an essential adaptation of obligate parasites in this family, which depend upon a host for survival. Several species of obligate parasites, including witchweeds (Striga, Alectra spp.) and broomrapes (Orobanche, Phelipanche spp.), are highly destructive agricultural weeds that pose a significant threat to global food security. Understanding how parasites sense SLs and other host-derived stimulants will catalyze the development of innovative chemical and biological control methods. This review synthesizes the recent discoveries of strigolactone receptors in parasitic Orobanchaceae, their signaling mechanism, and key steps in their evolution. Title: Desmethyl butenolides are optimal ligands for karrikin receptor proteins Yao J, Scaffidi A, Meng Y, Melville KT, Komatsu A, Khosla A, Nelson DC, Kyozuka J, Flematti GR, Waters MT Ref: New Phytol, :, 2021 : PubMed ESTHER: Yao_2021_New.Phytol__ PubMedSearch: Yao 2021 New.Phytol PubMedID: 33474738 Gene_locus related to this paper: arath-AtD14, arath-KAI2.D14L Inhibitor(s) related to this paper: 4-CN-desmethyl-Debranone, 4-CN-Debranone, GR24 Abstract Strigolactones and karrikins are butenolide molecules that regulate plant growth. They are perceived via the alpha/beta-hydrolase DWARF14 (D14) and its homologue KARRIKIN INSENSITIVE2 (KAI2), respectively. Plant-derived strigolactones have a butenolide ring with a methyl group that is essential for bioactivity. By contrast, karrikins are abiotic in origin, and the butenolide methyl group is non-essential. KAI2 is probably a receptor for an endogenous butenolide, but the identity of this compound remains unknown. Here we characterise the specificity of KAI2 towards differing butenolide ligands using genetic and biochemical approaches. We find that KAI2 proteins from multiple species are most sensitive to desmethyl butenolides that lack a methyl group. Desmethyl-GR24 and desmethyl-CN-debranone are active via KAI2 but not D14. They are more potent KAI2 agonists than their methyl-substituted reference compounds both in vitro and in plants. The preference of KAI2 for desmethyl butenolides is conserved in Selaginella moellendorffii and Marchantia polymorpha, suggesting that it is an ancient trait in land plant evolution. Our findings provide insight into the mechanistic basis for differential ligand perception by KAI2 and D14, and support the view that the endogenous substrates for KAI2 and D14 have distinct chemical structures and biosynthetic origins. Title: Strigolactone biosynthesis catalyzed by cytochrome P450 and sulfotransferase in sorghum Yoda A, Mori N, Akiyama K, Kikuchi M, Xie X, Miura K, Yoneyama K, Sato-Izawa K, Yamaguchi S and Nomura T <1 more author(s)> Yoda A, Mori N, Akiyama K, Kikuchi M, Xie X, Miura K, Yoneyama K, Sato-Izawa K, Yamaguchi S, Nelson DC, Nomura T (- 1) Ref: New Phytol, 232:1999, 2021 : PubMed ESTHER: Yoda_2021_New.Phytol_232_1999 PubMedSearch: Yoda 2021 New.Phytol 232 1999 PubMedID: 34525227 Abstract Root parasitic plants such as Striga, Orobanche, and Phelipanche spp. cause serious damage to crop production world-wide. Deletion of the Low Germination Stimulant 1 (LGS1) gene gives a Striga-resistance trait in sorghum (Sorghum bicolor). The LGS1 gene encodes a sulfotransferase-like protein, but its function has not been elucidated. Since the profile of strigolactones (SLs) that induce seed germination in root parasitic plants is altered in the lgs1 mutant, LGS1 is thought to be an SL biosynthetic enzyme. In order to clarify the enzymatic function of LGS1, we looked for candidate SL substrates that accumulate in the lgs1 mutants and performed in vivo and in vitro metabolism experiments. We found the SL precursor 18-hydroxycarlactonoic acid (18-OH-CLA) is a substrate for LGS1. CYP711A cytochrome P450 enzymes (SbMAX1 proteins) in sorghum produce 18-OH-CLA. When LGS1 and SbMAX1 coding sequences were co-expressed in Nicotiana benthamiana with the upstream SL biosynthesis genes from sorghum, the canonical SLs 5-deoxystrigol and 4-deoxyorobanchol were produced. This finding showed that LGS1 in sorghum uses a sulfo group to catalyze leaving of a hydroxyl group and cyclization of 18-OH-CLA. A similar SL biosynthetic pathway has not been found in other plant species. Title: Structure-Function Analysis of SMAX1 Reveals Domains That Mediate Its Karrikin-Induced Proteolysis and Interaction with the Receptor KAI2 Khosla A, Morffy N, Li Q, Faure L, Chang SH, Yao J, Zheng J, Cai ML, Stanga J and Nelson DC <2 more author(s)> Khosla A, Morffy N, Li Q, Faure L, Chang SH, Yao J, Zheng J, Cai ML, Stanga J, Flematti GR, Waters MT, Nelson DC (- 2) Ref: Plant Cell, 32:2639, 2020 : PubMed ESTHER: Khosla_2020_Plant.Cell_32_2639 PubMedSearch: Khosla 2020 Plant.Cell 32 2639 PubMedID: 32434855 Abstract Karrikins (KARs) are butenolides found in smoke that can influence germination and seedling development of many plants. The KAR signaling mechanism is hypothesized to be very similar to that of the plant hormone strigolactone (SL). Both pathways require the F-box protein MORE AXILLARY GROWTH2 (MAX2), and other core signaling components have shared ancestry. Putatively, KAR activates the receptor KARRIKIN INSENSITIVE2 (KAI2), triggering its association with the E3 ubiquitin ligase complex SCF(MAX2) and downstream targets SUPPRESSOR OF MAX2 1 (SMAX1) and SMAX1-LIKE2 (SMXL2). Polyubiquitination and proteolysis of SMAX1 and SMXL2 then enable growth responses to KAR. However, many of the assumptions of this model have not been demonstrated. Therefore, we investigated the posttranslational regulation of SMAX1 from the model plant Arabidopsis (Arabidopsis thaliana). We find evidence that SMAX1 is degraded by KAI2-SCF(MAX2) but is also subject to MAX2-independent turnover. We identify SMAX1 domains that are responsible for its nuclear localization, KAR-induced degradation, association with KAI2, and ability to interact with other SMXL proteins. KAI2 undergoes MAX2-independent degradation after KAR treatment, which we propose results from its association with SMAX1 and SMXL2. Finally, we discover an SMXL domain that mediates receptor-target interaction preferences in KAR and SL signaling, laying the foundation for understanding how these highly similar pathways evolved to fulfill different roles. Title: Evolution of strigolactone receptors by gradual neo-functionalization of KAI2 paralogues Bythell-Douglas R, Rothfels CJ, Stevenson DWD, Graham SW, Wong GK, Nelson DC, Bennett T Ref: BMC Biol, 15:52, 2017 : PubMed ESTHER: Bythell-Douglas_2017_BMC.Biol_15_52 PubMedSearch: Bythell-Douglas 2017 BMC.Biol 15 52 PubMedID: 28662667 Abstract BACKGROUND: Strigolactones (SLs) are a class of plant hormones that control many aspects of plant growth. The SL signalling mechanism is homologous to that of karrikins (KARs), smoke-derived compounds that stimulate seed germination. In angiosperms, the SL receptor is an alpha/beta-hydrolase known as DWARF14 (D14); its close homologue, KARRIKIN INSENSITIVE2 (KAI2), functions as a KAR receptor and likely recognizes an uncharacterized, endogenous signal ('KL'). Previous phylogenetic analyses have suggested that the KAI2 lineage is ancestral in land plants, and that canonical D14-type SL receptors only arose in seed plants; this is paradoxical, however, as non-vascular plants synthesize and respond to SLs. Title: The karrikin receptor KAI2 promotes drought resistance in Arabidopsis thaliana Li W, Nguyen KH, Chu HD, Ha CV, Watanabe Y, Osakabe Y, Leyva-Gonzalez MA, Sato M, Toyooka K and Tran LP <9 more author(s)> Li W, Nguyen KH, Chu HD, Ha CV, Watanabe Y, Osakabe Y, Leyva-Gonzalez MA, Sato M, Toyooka K, Voges L, Tanaka M, Mostofa MG, Seki M, Seo M, Yamaguchi S, Nelson DC, Tian C, Herrera-Estrella L, Tran LP (- 9) Ref: PLoS Genet, 13:e1007076, 2017 : PubMed ESTHER: Li_2017_PLoS.Genet_13_e1007076 PubMedSearch: Li 2017 PLoS.Genet 13 e1007076 PubMedID: 29131815 Gene_locus related to this paper: arath-KAI2.D14L Abstract Drought causes substantial reductions in crop yields worldwide. Therefore, we set out to identify new chemical and genetic factors that regulate drought resistance in Arabidopsis thaliana. Karrikins (KARs) are a class of butenolide compounds found in smoke that promote seed germination, and have been reported to improve seedling vigor under stressful growth conditions. Here, we discovered that mutations in KARRIKIN INSENSITIVE2 (KAI2), encoding the proposed karrikin receptor, result in hypersensitivity to water deprivation. We performed transcriptomic, physiological and biochemical analyses of kai2 plants to understand the basis for KAI2-regulated drought resistance. We found that kai2 mutants have increased rates of water loss and drought-induced cell membrane damage, enlarged stomatal apertures, and higher cuticular permeability. In addition, kai2 plants have reduced anthocyanin biosynthesis during drought, and are hyposensitive to abscisic acid (ABA) in stomatal closure and cotyledon opening assays. We identified genes that are likely associated with the observed physiological and biochemical changes through a genome-wide transcriptome analysis of kai2 under both well-watered and dehydration conditions. These data provide evidence for crosstalk between ABA- and KAI2-dependent signaling pathways in regulating plant responses to drought. A comparison of the strigolactone receptor mutant d14 (DWARF14) to kai2 indicated that strigolactones also contributes to plant drought adaptation, although not by affecting cuticle development. Our findings suggest that chemical or genetic manipulation of KAI2 and D14 signaling may provide novel ways to improve drought resistance. Title: Strigolactone Signaling and Evolution Waters MT, Gutjahr C, Bennett T, Nelson DC Ref: Annu Rev Plant Biol, 68:291, 2017 : PubMed ESTHER: Waters_2017_Annu.Rev.Plant.Biol_68_291 PubMedSearch: Waters 2017 Annu.Rev.Plant.Biol 68 291 PubMedID: 28125281 Abstract Strigolactones are a structurally diverse class of plant hormones that control many aspects of shoot and root growth. Strigolactones are also exuded by plants into the rhizosphere, where they promote symbiotic interactions with arbuscular mycorrhizal fungi and germination of root parasitic plants in the Orobanchaceae family. Therefore, understanding how strigolactones are made, transported, and perceived may lead to agricultural innovations as well as a deeper knowledge of how plants function. Substantial progress has been made in these areas over the past decade. In this review, we focus on the molecular mechanisms, core developmental roles, and evolutionary history of strigolactone signaling. We also propose potential translational applications of strigolactone research to agriculture. Title: Structural modelling and transcriptional responses highlight a clade of PpKAI2-LIKE genes as candidate receptors for strigolactones in Physcomitrella patens Lopez-Obando M, Conn CE, Hoffmann B, Bythell-Douglas R, Nelson DC, Rameau C, Bonhomme S Ref: Planta, 243:1441, 2016 : PubMed ESTHER: Lopez-Obando_2016_Planta_243_1441 PubMedSearch: Lopez-Obando 2016 Planta 243 1441 PubMedID: 26979323 Abstract MAIN CONCLUSION: A set of PpKAI2 - LIKE paralogs that may encode strigolactone receptors in Physcomitrella patens were identified through evolutionary, structural, and transcriptional analyses, suggesting that strigolactone perception may have evolved independently in basal land plants in a similar manner as spermatophytes. Carotenoid-derived compounds known as strigolactones are a new class of plant hormones that modulate development and interactions with parasitic plants and arbuscular mycorrhizal fungi. The strigolactone receptor protein DWARF14 (D14) belongs to the alpha/beta hydrolase family. D14 is closely related to KARRIKIN INSENSITIVE2 (KAI2), a receptor of smoke-derived germination stimulants called karrikins. Strigolactone and karrikin structures share a butenolide ring that is necessary for bioactivity. Charophyte algae and basal land plants produce strigolactones that influence their development. However phylogenetic studies suggest that D14 is absent from algae, moss, and liverwort genomes, raising the question of how these basal plants perceive strigolactones. Strigolactone perception during seed germination putatively evolved in parasitic plants through gene duplication and neofunctionalization of KAI2 paralogs. The moss Physcomitrella patens shows an increase in KAI2 gene copy number, similar to parasitic plants. In this study we investigated whether P. patens KAI2-LIKE (PpKAI2L) genes may contribute to strigolactone perception. Based on phylogenetic analyses and homology modelling, we predict that a clade of PpKAI2L proteins have enlarged ligand-binding cavities, similar to D14. We observed that some PpKAI2L genes have transcriptional responses to the synthetic strigolactone GR24 racemate or its enantiomers. These responses were influenced by light and dark conditions. Moreover, (+)-GR24 seems to be the active enantiomer that induces the transcriptional responses of PpKAI2L genes. We hypothesize that members of specific PpKAI2L clades are candidate strigolactone receptors in moss. Title: Smoke and Hormone Mirrors: Action and Evolution of Karrikin and Strigolactone Signaling Morffy N, Faure L, Nelson DC Ref: Trends Genet, 32:176, 2016 : PubMed ESTHER: Morffy_2016_Trends.Genet_32_176 PubMedSearch: Morffy 2016 Trends.Genet 32 176 PubMedID: 26851153 Inhibitor(s) related to this paper: GR24 Abstract Karrikins and strigolactones are two classes of butenolide molecules that have diverse effects on plant growth. Karrikins are found in smoke and strigolactones are plant hormones, yet both molecules are likely recognized through highly similar signaling mechanisms. Here we review the most recent discoveries of karrikin and strigolactone perception and signal transduction. Two paralogous alpha/beta hydrolases, KAI2 and D14, are respectively karrikin and strigolactone receptors. D14 acts with an F-box protein, MAX2, to target SMXL/D53 family proteins for proteasomal degradation, and genetic data suggest that KAI2 acts similarly. There are striking parallels in the signaling mechanisms of karrikins, strigolactones, and other plant hormones, including auxins, jasmonates, and gibberellins. Recent investigations of host perception in parasitic plants have demonstrated that strigolactone recognition can evolve following gene duplication of KAI2. Title: Functional redundancy in the control of seedling growth by the karrikin signaling pathway Stanga JP, Morffy N, Nelson DC Ref: Planta, 243:1397, 2016 : PubMed ESTHER: Stanga_2016_Planta_243_1397 PubMedSearch: Stanga 2016 Planta 243 1397 PubMedID: 26754282 Abstract MAIN CONCLUSION: SMAX1 and SMXL2 control seedling growth, demonstrating functional redundancy within a gene family that mediates karrikin and strigolactone responses. Strigolactones (SLs) are plant hormones with butenolide moieties that control diverse aspects of plant growth, including shoot branching. Karrikins (KARs) are butenolide molecules found in smoke that enhance seed germination and seedling photomorphogenesis. In Arabidopsis thaliana, SLs and KARs signal through the alpha/beta hydrolases D14 and KAI2, respectively. The F-box protein MAX2 is essential for both signaling pathways. SUPPRESSOR OF MAX2 1 (SMAX1) plays a prominent role in KAR-regulated growth downstream of MAX2, and SMAX1-LIKE genes SMXL6, SMXL7, and SMXL8 mediate SL responses. We previously found that smax1 loss-of-function mutants display constitutive KAR response phenotypes, including reduced seed dormancy and hypersensitive growth responses to light in seedlings. However, smax1 seedlings remain slightly responsive to KARs, suggesting that there is functional redundancy in karrikin signaling. SMXL2 is a strong candidate for this redundancy because it is the closest paralog of SMAX1, and because its expression is regulated by KAR signaling. Here, we present evidence that SMXL2 controls hypocotyl growth and expression of the KAR/SL transcriptional markers KUF1, IAA1, and DLK2 redundantly with SMAX1. Hypocotyl growth in the smax1 smxl2 double mutant is insensitive to KAR and SL, and etiolated smax1 smxl2 seedlings have reduced hypocotyl elongation. However, smxl2 has little or no effect on seed germination, leaf shape, or petiole orientation, which appear to be predominantly controlled by SMAX1. Neither SMAX1 nor SMXL2 affect axillary branching or inflorescence height, traits that are under SL control. These data support the model that karrikin and strigolactone responses are mediated by distinct subclades of the SMXL family, and further the case for parallel butenolide signaling pathways that evolved through ancient KAI2 and SMXL duplications. Title: PLANT EVOLUTION. Convergent evolution of strigolactone perception enabled host detection in parasitic plants Conn CE, Bythell-Douglas R, Neumann D, Yoshida S, Whittington B, Westwood JH, Shirasu K, Bond CS, Dyer KA, Nelson DC Ref: Science, 349:540, 2015 : PubMed ESTHER: Conn_2015_Science_349_540 PubMedSearch: Conn 2015 Science 349 540 PubMedID: 26228149 Gene_locus related to this paper: phera-PrKAI2c, phera-PrKAI2d1, phera-PrKAI2d2, phera-PrKAI2d3, phera-PrKAI2d4, strhe-ShD14, orocc-OcKAI2d2, trivs-TvKAI2c, strhe-ShKAI2D2, 9lami-a0a2u8xq24, orocc-OcD14, conam-CaKAI2c, 9lami-a0a2u8xq49, 9lami-a0a2u8xq53, oroce-OcKAI2d2, oroce-OcKAI2d3, orocc-OcKAI2d4, orocc-OcKAI2d1, 9lami-a0a2u8xqa1, oroce-OcD14, 9lami-a0a2u8xqb0, strhe-sHKAI2d1, conam-CaD14, 9lami-a0a2u8xqc8, 9lami-a0a2u8xqd2, 9lami-a0a2u8xqe1, 9lami-a0a2u8xqh0, oroce-OcKAI2d1, orocc-OcKAI2c, strhe-ShKAI2c, 9lami-a0a2u8xqv8, orocc-OcKAI2d6, orocc-OcKAI2d5, 9lami-a0a2u8xr73, oroce-OcKAI2c, 9lami-a0a2u8xr89, orocc-OcKAI2d3, 9lami-a0a2u8xrl6, strhe-ShKAI2i, 9lami-a0a2u8xrn7 Abstract Obligate parasitic plants in the Orobanchaceae germinate after sensing plant hormones, strigolactones, exuded from host roots. In Arabidopsis thaliana, the alpha/beta-hydrolase D14 acts as a strigolactone receptor that controls shoot branching, whereas its ancestral paralog, KAI2, mediates karrikin-specific germination responses. We observed that KAI2, but not D14, is present at higher copy numbers in parasitic species than in nonparasitic relatives. KAI2 paralogs in parasites are distributed into three phylogenetic clades. The fastest-evolving clade, KAI2d, contains the majority of KAI2 paralogs. Homology models predict that the ligand-binding pockets of KAI2d resemble D14. KAI2d transgenes confer strigolactone-specific germination responses to Arabidopsis thaliana. Thus, the KAI2 paralogs D14 and KAI2d underwent convergent evolution of strigolactone recognition, respectively enabling developmental responses to strigolactones in angiosperms and host detection in parasites. Title: Evidence that KARRIKIN-INSENSITIVE2 (KAI2) Receptors may Perceive an Unknown Signal that is not Karrikin or Strigolactone Conn CE, Nelson DC Ref: Front Plant Sci, 6:1219, 2015 : PubMed ESTHER: Conn_2015_Front.Plant.Sci_6_1219 PubMedSearch: Conn 2015 Front.Plant.Sci 6 1219 PubMedID: 26779242 Abstract The alpha/beta-hydrolases KAI2 and D14 are paralogous receptors for karrikins and strigolactones, two classes of plant growth regulators with butenolide moieties. KAI2 and D14 act in parallel signaling pathways that share a requirement for the F-box protein MAX2, but produce distinct growth responses by regulating different members of the SMAX1-LIKE/D53 family. kai2 and max2 mutants share seed germination, seedling growth, leaf shape, and petiole orientation phenotypes that are not found in d14 or SL-deficient mutants. This implies that KAI2 recognizes an unknown, endogenous signal, herein termed KAI2 ligand (KL). Recent studies of ligand-specificity among KAI2 paralogs in basal land plants and root parasitic plants suggest that karrikin and strigolactone perception may be evolutionary adaptations of KL receptors. Here we demonstrate that evolutionarily conserved KAI2c genes from two parasite species rescue multiple phenotypes of the Arabidopsis kai2 mutant, unlike karrikin-, and strigolactone-specific KAI2 paralogs. We hypothesize that KAI2c proteins recognize KL, which could be an undiscovered hormone. Title: SMAX1-LIKE/D53 Family Members Enable Distinct MAX2-Dependent Responses to Strigolactones and Karrikins in Arabidopsis Soundappan I, Bennett T, Morffy N, Liang Y, Stanga JP, Abbas A, Leyser O, Nelson DC Ref: Plant Cell, 27:3143, 2015 : PubMed ESTHER: Soundappan_2015_Plant.Cell_27_3143 PubMedSearch: Soundappan 2015 Plant.Cell 27 3143 PubMedID: 26546447 Abstract The plant hormones strigolactones and smoke-derived karrikins are butenolide signals that control distinct aspects of plant development. Perception of both molecules in Arabidopsis thaliana requires the F-box protein MORE AXILLARY GROWTH2 (MAX2). Recent studies suggest that the homologous SUPPRESSOR OF MAX2 1 (SMAX1) in Arabidopsis and DWARF53 (D53) in rice (Oryza sativa) are downstream targets of MAX2. Through an extensive analysis of loss-of-function mutants, we demonstrate that the Arabidopsis SMAX1-LIKE genes SMXL6, SMXL7, and SMXL8 are co-orthologs of rice D53 that promote shoot branching. SMXL7 is degraded rapidly after treatment with the synthetic strigolactone mixture rac-GR24. Like D53, SMXL7 degradation is MAX2- and D14-dependent and can be prevented by deletion of a putative P-loop. Loss of SMXL6,7,8 suppresses several other strigolactone-related phenotypes in max2, including increased auxin transport and PIN1 accumulation, and increased lateral root density. Although only SMAX1 regulates germination and hypocotyl elongation, SMAX1 and SMXL6,7,8 have complementary roles in the control of leaf morphology. Our data indicate that SMAX1 and SMXL6,7,8 repress karrikin and strigolactone signaling, respectively, and suggest that all MAX2-dependent growth effects are mediated by degradation of SMAX1/SMXL proteins. We propose that functional diversification within the SMXL family enabled responses to different butenolide signals through a shared regulatory mechanism. Title: SUPPRESSOR OF MORE AXILLARY GROWTH2 1 controls seed germination and seedling development in Arabidopsis Stanga JP, Smith SM, Briggs WR, Nelson DC Ref: Plant Physiol, 163:318, 2013 : PubMed ESTHER: Stanga_2013_Plant.Physiol_163_318 PubMedSearch: Stanga 2013 Plant.Physiol 163 318 PubMedID: 23893171 Abstract Abiotic chemical signals discovered in smoke that are known as karrikins (KARs) and the endogenous hormone strigolactone (SL) control plant growth through a shared MORE AXILLARY GROWTH2 (MAX2)-dependent pathway. A SL biosynthetic pathway and candidate KAR/SL receptors have been characterized, but signaling downstream of MAX2 is poorly defined. A screen for genetic suppressors of the enhanced seed dormancy phenotype of max2 in Arabidopsis (Arabidopsis thaliana) led to identification of a suppressor of max2 1 (smax1) mutant. smax1 restores the seed germination and seedling photomorphogenesis phenotypes of max2 but does not affect the lateral root formation, axillary shoot growth, or senescence phenotypes of max2. Expression of three transcriptional markers of KAR/SL signaling, D14-LIKE2, KAR-UP F-BOX1, and INDOLE-3-ACETIC ACID INDUCIBLE1, is rescued in smax1 max2 seedlings. SMAX1 is a member of an eight-gene family in Arabidopsis that has weak similarity to HEAT SHOCK PROTEIN 101, which encodes a caseinolytic peptidase B chaperonin required for thermotolerance. SMAX1 and the SMAX1-like (SMXL) homologs are differentially expressed in Arabidopsis tissues. SMAX1 transcripts are most abundant in dry seed, consistent with its function in seed germination control. Several SMXL genes are up-regulated in seedlings treated with the synthetic SL GR24. SMAX1 and SMXL2 transcripts are reduced in max2 seedlings, which could indicate negative feedback regulation by KAR/SL signaling. smax1 seed and seedling growth mimics the wild type treated with KAR/SL, but smax1 seedlings are still responsive to 2H-furo[2,3-c]pyran-2-one (KAR2) or GR24. We conclude that SMAX1 is an important component of KAR/SL signaling during seed germination and seedling growth but is not necessary for all MAX2-dependent responses. We hypothesize that one or more SMXL proteins may also act downstream of MAX2 to control the diverse developmental responses to KARs and SLs. Title: Regulation of seed germination and seedling growth by chemical signals from burning vegetation Nelson DC, Flematti GR, Ghisalberti EL, Dixon KW, Smith SM Ref: Annu Rev Plant Biol, 63:107, 2012 : PubMed ESTHER: Nelson_2012_Annu.Rev.Plant.Biol_63_107 PubMedSearch: Nelson 2012 Annu.Rev.Plant.Biol 63 107 PubMedID: 22404467 Abstract It is well known that burning of vegetation stimulates new plant growth and landscape regeneration. The discovery that char and smoke from such fires promote seed germination in many species indicates the presence of chemical stimulants. Nitrogen oxides stimulate seed germination, but their importance in post-fire germination has been questioned. Cyanohydrins have been recently identified in aqueous smoke solutions and shown to stimulate germination of some species through the slow release of cyanide. However, the most information is available for karrikins, a family of butenolides related to 3-methyl-2H-furo[2,3-c]pyran-2-one. Karrikins stimulate seed germination and influence seedling growth. They are active in species not normally associated with fire, and in Arabidopsis they require the F-box protein MAX2, which also controls responses to strigolactone hormones. We hypothesize that chemical similarity between karrikins and strigolactones provided the opportunity for plants to employ a common signal transduction pathway to respond to both types of compound, while tailoring specific developmental responses to these distinct environmental signals. Title: Specialisation within the DWARF14 protein family confers distinct responses to karrikins and strigolactones in Arabidopsis. Waters MT, Nelson DC, Scaffidi A, Flematti GR, Sun YK, Dixon KW, Smith SM Ref: Development, 139:1285, 2012 : PubMed ESTHER: Waters_2012_Development_139_1285 PubMedSearch: Waters 2012 Development 139 1285 PubMedID: 22357928 Gene_locus related to this paper: arath-AtD14, arath-KAI2.D14L, orysj-q10j20, orysj-Q10QA5 Abstract Karrikins are butenolides derived from burnt vegetation that stimulate seed germination and enhance seedling responses to light. Strigolactones are endogenous butenolide hormones that regulate shoot and root architecture, and stimulate the branching of arbuscular mycorrhizal fungi. Thus, karrikins and strigolactones are structurally similar but physiologically distinct plant growth regulators. In Arabidopsis thaliana, responses to both classes of butenolides require the F-box protein MAX2, but it remains unclear how discrete responses to karrikins and strigolactones are achieved. In rice, the DWARF14 protein is required for strigolactone-dependent inhibition of shoot branching. Here, we show that the Arabidopsis DWARF14 orthologue, AtD14, is also necessary for normal strigolactone responses in seedlings and adult plants. However, the AtD14 paralogue KARRIKIN INSENSITIVE 2 (KAI2) is specifically required for responses to karrikins, and not to strigolactones. Phylogenetic analysis indicates that KAI2 is ancestral and that AtD14 functional specialisation has evolved subsequently. Atd14 and kai2 mutants exhibit distinct subsets of max2 phenotypes, and expression patterns of AtD14 and KAI2 are consistent with the capacity to respond to either strigolactones or karrikins at different stages of plant development. We propose that AtD14 and KAI2 define a class of proteins that permit the separate regulation of karrikin and strigolactone signalling by MAX2. Our results support the existence of an endogenous, butenolide-based signalling mechanism that is distinct from the strigolactone pathway, providing a molecular basis for the adaptive response of plants to smoke. Title: F-box protein MAX2 has dual roles in karrikin and strigolactone signaling in Arabidopsis thaliana Nelson DC, Scaffidi A, Dun EA, Waters MT, Flematti GR, Dixon KW, Beveridge CA, Ghisalberti EL, Smith SM Ref: Proc Natl Acad Sci U S A, 108:8897, 2011 : PubMed ESTHER: Nelson_2011_Proc.Natl.Acad.Sci.U.S.A_108_8897 PubMedSearch: Nelson 2011 Proc.Natl.Acad.Sci.U.S.A 108 8897 PubMedID: 21555559 Abstract Smoke is an important abiotic cue for plant regeneration in postfire landscapes. Karrikins are a class of compounds discovered in smoke that promote seed germination and influence early development of many plants by an unknown mechanism. A genetic screen for karrikin-insensitive mutants in Arabidopsis thaliana revealed that karrikin signaling requires the F-box protein MAX2, which also mediates responses to the structurally-related strigolactone family of phytohormones. Karrikins and the synthetic strigolactone GR24 trigger similar effects on seed germination, seedling photomorphogenesis, and expression of a small set of genes during these developmental stages. Karrikins also repress MAX4 and IAA1 transcripts, which show negative feedback regulation by strigolactone. We demonstrate that all of these common responses are abolished in max2 mutants. Unlike strigolactones, however, karrikins do not inhibit shoot branching in Arabidopsis or pea, indicating that plants can distinguish between these signals. These results suggest that a MAX2-dependent signal transduction mechanism was adapted to mediate responses to two chemical cues with distinct roles in plant ecology and development. Title: Smoke signals and seed dormancy: where next for MAX2? Waters MT, Smith SM, Nelson DC Ref: Plant Signal Behav, 6:1418, 2011 : PubMed ESTHER: Waters_2011_Plant.Signal.Behav_6_1418 PubMedSearch: Waters 2011 Plant.Signal.Behav 6 1418 PubMedID: 22019642 Abstract The Arabidopsis thaliana F-box protein MAX2 has been discovered in four separate genetic screens, indicating that it has roles in leaf senescence, seedling photosensitivity, shoot outgrowth, and seed germination. Both strigolactones and karrikins can regulate A. thaliana seed germination and seedling photomorphogenesis in a MAX2-dependent manner, but only strigolactones inhibit shoot branching. How MAX2 mediates specific responses to both classes of structurally-related signals, and the origin of its dual role remains unknown. The moss Physcomitrella patens utilizes strigolactones and MAX2 orthologs are present across the land plants, suggesting that this signaling system could have an ancient origin. The seed of parasitic Orobanchaceae species germinate preferentially in response to strigolactones over karrikins, and putative Orobanchaceae MAX2 orthologs form a sub-clade distinct from those of other dicots. These observations suggest that lineage-specific evolution of MAX2 may have given rise to specialized responses to these signaling molecules. Title: Structure-activity relationship of karrikin germination stimulants Flematti GR, Scaffidi A, Goddard-Borger ED, Heath CH, Nelson DC, Commander LE, Stick RV, Dixon KW, Smith SM, Ghisalberti EL Ref: Journal of Agricultural and Food Chemistry, 58:8612, 2010 : PubMed ESTHER: Flematti_2010_J.Agric.Food.Chem_58_8612 PubMedSearch: Flematti 2010 J.Agric.Food.Chem 58 8612 PubMedID: 20617827 Abstract Karrikins (2H-furo[2,3-c]pyran-2-ones) are potent smoke-derived germination promoters for a diverse range of plant species but, to date, their mode of action remains unknown. This paper reports the structure-activity relationship of numerous karrikin analogues to increase understanding of the key structural features of the molecule that are required for biological activity. The results demonstrate that modification at the C5 position is preferred over modification at the C3, C4, or C7 positions for retaining the highest bioactivity. Title: Karrikins enhance light responses during germination and seedling development in Arabidopsis thaliana Nelson DC, Flematti GR, Riseborough JA, Ghisalberti EL, Dixon KW, Smith SM Ref: Proc Natl Acad Sci U S A, 107:7095, 2010 : PubMed ESTHER: Nelson_2010_Proc.Natl.Acad.Sci.U.S.A_107_7095 PubMedSearch: Nelson 2010 Proc.Natl.Acad.Sci.U.S.A 107 7095 PubMedID: 20351290 Abstract Karrikins are a class of seed germination stimulants identified in smoke from wildfires. Microarray analysis of imbibed Arabidopsis thaliana seeds was performed to identify transcriptional responses to KAR(1) before germination. A small set of genes that are regulated by KAR(1), even when germination is prevented by the absence of gibberellin biosynthesis or light, were identified. Light-induced genes, putative HY5-binding targets, and ABRE-like promoter motifs were overrepresented among KAR(1)-up-regulated genes. KAR(1) transiently induced the light signal transduction transcription factor genes HY5 and HYH. Germination of afterripened Arabidopsis seed was triggered at lower fluences of red light when treated with KAR(1). Light-dependent cotyledon expansion and inhibition of hypocotyl elongation were enhanced in the presence of germination-active karrikins. HY5 is important for the Arabidopsis hypocotyl elongation, but not seed germination, response to karrikins. These results reveal a role for karrikins in priming light responses in the emerging seedling, and suggest that the influence of karrikins on postfire ecology may not be limited to germination recruitment. Title: Karrikins: A New Family of Plant Growth Regulators in Smoke Chiwocha SDS, Dixon KW, Flematti GR, Ghisalberti EL, Merritt DJ, Nelson DC, Riseborough JAM, Smith SM, Stevens JC Ref: Plant Sci, 177:252, 2009 : PubMed ESTHER: Chiwocha_2009_Plant.Sci_177_252 PubMedSearch: Chiwocha 2009 Plant.Sci 177 252 Abstract Karrikins are a chemically defined family of plant growth regulators discovered in smoke from burning plant material. Karrikins are potent in breaking dormancy of seeds of many species adapted to environments that regularly experience fire and smoke. The recent discovery that karrikins trigger seed germination and control seedling growth in taxa that would rarely experience fire indicates that their significance could extend far beyond fire ecology. This is exemplified by new studies showing that seeds of Arabidopsis thaliana respond sensitively and specifically to karrikins in smoke. These exciting discoveries might be explained if karrikins are produced in the environment by processes other than fire, such as by chemical or microbial degradation of vegetation in response to disturbance of the soil or removal of the plant canopy. Another hypothesis is that plants contain endogenous karrikins that function naturally in the control of seed germination and that species from fire-prone habitats have evolved to respond also to exogenous karrikins. A variant on this hypothesis is that karrikins mimic endogenous plant hormones such as terpenoids that control seed germination. The evidence for these hypotheses is discussed, but whatever the explanation karrikins are now firmly established as an important family of naturally occurring plant growth regulators. Title: Karrikins discovered in smoke trigger Arabidopsis seed germination by a mechanism requiring gibberellic acid synthesis and light Nelson DC, Riseborough JA, Flematti GR, Stevens J, Ghisalberti EL, Dixon KW, Smith SM Ref: Plant Physiol, 149:863, 2009 : PubMed ESTHER: Nelson_2009_Plant.Physiol_149_863 PubMedSearch: Nelson 2009 Plant.Physiol 149 863 PubMedID: 19074625 Abstract Discovery of the primary seed germination stimulant in smoke, 3-methyl-2H-furo[2,3-c]pyran-2-one (KAR1), has resulted in identification of a family of structurally related plant growth regulators, karrikins. KAR1 acts as a key germination trigger for many species from fire-prone, Mediterranean climates, but a molecular mechanism for this response remains unknown. We demonstrate that Arabidopsis (Arabidopsis thaliana), an ephemeral of the temperate northern hemisphere that has never, to our knowledge, been reported to be responsive to fire or smoke, rapidly and sensitively perceives karrikins. Thus, these signaling molecules may have greater significance among angiosperms than previously realized. Karrikins can trigger germination of primary dormant Arabidopsis seeds far more effectively than known phytohormones or the structurally related strigolactone GR-24. Natural variation and depth of seed dormancy affect the degree of KAR1 stimulation. Analysis of phytohormone mutant germination reveals suppression of KAR1 responses by abscisic acid and a requirement for gibberellin (GA) synthesis. The reduced germination of sleepy1 mutants is partially recovered by KAR1, which suggests that germination enhancement by karrikin is only partly DELLA dependent. While KAR1 has little effect on sensitivity to exogenous GA, it enhances expression of the GA biosynthetic genes GA3ox1 and GA3ox2 during seed imbibition. Neither abscisic acid nor GA levels in seed are appreciably affected by KAR1 treatment prior to radicle emergence, despite marked differences in germination outcome. KAR1 stimulation of Arabidopsis germination is light-dependent and reversible by far-red exposure, although limited induction of GA3ox1 still occurs in the dark. The observed requirements for light and GA biosynthesis provide the first insights into the karrikin mode of action. | |||||||
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